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The role of cis regulatory evolution in maize domestication.

Lemmon ZH, Bukowski R, Sun Q, Doebley JF - PLoS Genet. (2014)

Bottom Line: Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not.We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression.Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, University of Wisconsin - Madison, Madison, Wisconsin, United States of America.

ABSTRACT
Gene expression differences between divergent lineages caused by modification of cis regulatory elements are thought to be important in evolution. We assayed genome-wide cis and trans regulatory differences between maize and its wild progenitor, teosinte, using deep RNA sequencing in F1 hybrid and parent inbred lines for three tissue types (ear, leaf and stem). Pervasive regulatory variation was observed with approximately 70% of ∼17,000 genes showing evidence of regulatory divergence between maize and teosinte. However, many fewer genes (1,079 genes) show consistent cis differences with all sampled maize and teosinte lines. For ∼70% of these 1,079 genes, the cis differences are specific to a single tissue. The number of genes with cis regulatory differences is greatest for ear tissue, which underwent a drastic transformation in form during domestication. As expected from the domestication bottleneck, maize possesses less cis regulatory variation than teosinte with this deficit greatest for genes showing maize-teosinte cis regulatory divergence, suggesting selection on cis regulatory differences during domestication. Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not. We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression. Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.

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Overlap of genes assessed in the three tissues overall and in the CCT-AB gene list.Each compartment of the Venn diagram contains the tissue combination on top, number of genes overall in the middle, and number of genes from the CCT-AB gene list on bottom. CCT-AB overlap numbers marked by an “*” indicate significantly more overlap than expected by chance (permutation tests, p<1e-5). In the overall analysis the vast majority of genes (82%) were assayed in all three tissues. While this percent is much smaller for the CCT-AB candidate gene list (∼7%), this is still more of an overlap than expected by chance. The much higher degree of overlap of CCT-AB genes than expected suggests some CREs act in multiple tissues. Additionally, there are also many single tissue CCT-AB genes, which points towards the many cis elements that appear to function in tissue specific patterns.
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pgen-1004745-g001: Overlap of genes assessed in the three tissues overall and in the CCT-AB gene list.Each compartment of the Venn diagram contains the tissue combination on top, number of genes overall in the middle, and number of genes from the CCT-AB gene list on bottom. CCT-AB overlap numbers marked by an “*” indicate significantly more overlap than expected by chance (permutation tests, p<1e-5). In the overall analysis the vast majority of genes (82%) were assayed in all three tissues. While this percent is much smaller for the CCT-AB candidate gene list (∼7%), this is still more of an overlap than expected by chance. The much higher degree of overlap of CCT-AB genes than expected suggests some CREs act in multiple tissues. Additionally, there are also many single tissue CCT-AB genes, which points towards the many cis elements that appear to function in tissue specific patterns.

Mentions: RNAseq reads for all 29 F1 hybrids and 15 parents that aligned to segregating sites in the transcriptomes represent 23,816, 24,055, and 24,643 genes for ear, leaf and stem tissues, respectively (Table 2). The union of these three groups is 25,619 genes, which is 65% of the 39,423 genes from the maize filtered gene set (version 5b). We applied a filter to this list, requiring a read depth of 100 in both the parent inbreds and F1 hybrids. This filter reduced the lists to 15,939, 15,931, and 16,018 genes in ear, leaf, and stem tissues, respectively. The union of these three groups is 17,579 genes or ∼45% of the filtered gene set. There is a large degree of overlap among the genes expressed in the three tissues with 14,421 of 17,579 genes (82%) seen in all three tissues. Of the remaining genes, 1,467 are in two tissues and 1,691 are in only a single tissue (Figure 1).


The role of cis regulatory evolution in maize domestication.

Lemmon ZH, Bukowski R, Sun Q, Doebley JF - PLoS Genet. (2014)

Overlap of genes assessed in the three tissues overall and in the CCT-AB gene list.Each compartment of the Venn diagram contains the tissue combination on top, number of genes overall in the middle, and number of genes from the CCT-AB gene list on bottom. CCT-AB overlap numbers marked by an “*” indicate significantly more overlap than expected by chance (permutation tests, p<1e-5). In the overall analysis the vast majority of genes (82%) were assayed in all three tissues. While this percent is much smaller for the CCT-AB candidate gene list (∼7%), this is still more of an overlap than expected by chance. The much higher degree of overlap of CCT-AB genes than expected suggests some CREs act in multiple tissues. Additionally, there are also many single tissue CCT-AB genes, which points towards the many cis elements that appear to function in tissue specific patterns.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4222645&req=5

pgen-1004745-g001: Overlap of genes assessed in the three tissues overall and in the CCT-AB gene list.Each compartment of the Venn diagram contains the tissue combination on top, number of genes overall in the middle, and number of genes from the CCT-AB gene list on bottom. CCT-AB overlap numbers marked by an “*” indicate significantly more overlap than expected by chance (permutation tests, p<1e-5). In the overall analysis the vast majority of genes (82%) were assayed in all three tissues. While this percent is much smaller for the CCT-AB candidate gene list (∼7%), this is still more of an overlap than expected by chance. The much higher degree of overlap of CCT-AB genes than expected suggests some CREs act in multiple tissues. Additionally, there are also many single tissue CCT-AB genes, which points towards the many cis elements that appear to function in tissue specific patterns.
Mentions: RNAseq reads for all 29 F1 hybrids and 15 parents that aligned to segregating sites in the transcriptomes represent 23,816, 24,055, and 24,643 genes for ear, leaf and stem tissues, respectively (Table 2). The union of these three groups is 25,619 genes, which is 65% of the 39,423 genes from the maize filtered gene set (version 5b). We applied a filter to this list, requiring a read depth of 100 in both the parent inbreds and F1 hybrids. This filter reduced the lists to 15,939, 15,931, and 16,018 genes in ear, leaf, and stem tissues, respectively. The union of these three groups is 17,579 genes or ∼45% of the filtered gene set. There is a large degree of overlap among the genes expressed in the three tissues with 14,421 of 17,579 genes (82%) seen in all three tissues. Of the remaining genes, 1,467 are in two tissues and 1,691 are in only a single tissue (Figure 1).

Bottom Line: Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not.We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression.Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, University of Wisconsin - Madison, Madison, Wisconsin, United States of America.

ABSTRACT
Gene expression differences between divergent lineages caused by modification of cis regulatory elements are thought to be important in evolution. We assayed genome-wide cis and trans regulatory differences between maize and its wild progenitor, teosinte, using deep RNA sequencing in F1 hybrid and parent inbred lines for three tissue types (ear, leaf and stem). Pervasive regulatory variation was observed with approximately 70% of ∼17,000 genes showing evidence of regulatory divergence between maize and teosinte. However, many fewer genes (1,079 genes) show consistent cis differences with all sampled maize and teosinte lines. For ∼70% of these 1,079 genes, the cis differences are specific to a single tissue. The number of genes with cis regulatory differences is greatest for ear tissue, which underwent a drastic transformation in form during domestication. As expected from the domestication bottleneck, maize possesses less cis regulatory variation than teosinte with this deficit greatest for genes showing maize-teosinte cis regulatory divergence, suggesting selection on cis regulatory differences during domestication. Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not. We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression. Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.

Show MeSH
Related in: MedlinePlus